Advancing the science and practice of rare plant conservation with the Center for Plant Conservation Reintroduction Database.

Premise: Reintroductions or translocations are an increasingly important activity to recover and conserve at-risk plant species. Yet because many are not published in the scientific literature, learning from previous attempts may often require considerable time and effort. The Center for Plant Conservation Reintroduction Database (CPCRD; https://saveplants.org/reintroduction-database/), a new centralized and standardized repository of U.S.-based plant reintroductions, aims to improve the efficiency and effectiveness of accessing data on rare plant reintroductions. Methods: The CPCRD is the product of multiple efforts to assemble information on rare plant reintroductions in the United States. The database comprises a wealth of standardized data on the key stages of a reintroduction, from the planning and implementation phases, to monitoring and management techniques. Results: The CPCRD is a dynamic resource, allowing data contributors to continually update their entries as projects progress. While contributions are ongoing, the CPCRD currently includes 460 projects involving 201 plant taxa, spanning diverse growth forms, ecosystems, and regions. Discussion: The CPCRD and its well-documented and monitored projects provide a valuable practical resource for conservation practitioners, and have supported multiple scientific studies and contributed to the internationally recognized Center for Plant Conservation Best Practices Guidelines.

Development of a Micropropagation Protocol for the Ex Situ Conservation of Nuttall's Scrub Oak (Quercus dumosa).

Worldwide, oak species are threatened with extinction due to habitat loss, pathogens, and changing fire regimes. Ex situ conservation through tissue culture may protect the remaining genetic diversity of Quercus dumosa, or the coastal sage scrub oak, from further loss. We designed three basal salt formulations based on the mineral composition of shoot tips and first leaves from mature Q. dumosa and explored carbohydrate source, stress-mitigating compounds, and plant growth regulator concentrations to develop a method of cultivating many Q. dumosa culture lines in vitro. All three novel basal salt formulations led to decreased necrosis compared with commercial basal salt formulas WPM, MS, and DKW. Substitution of 30 g L-1 sucrose with glucose and adding 250 mg L-1 ascorbic acid, 5.2 mg L-1 SNP sodium nitroprusside, and 103 mg L-1 y-aminobutyric acid improved culture health overall. In an experiment involving 115 culture lines, 0.66 mg L-1 6-benzylaminopurine produced the highest average shoots per explant, but 0.33 mg L-1 produced the greatest proportion of shoots 2 cm or greater. Incubation for 24 h in 20 mg L-1 indole-3-butyric acid led to the most rooting. These methods show promise for the ex situ conservation of many genotypes of endangered Q. dumosa.

Identifying predictors of translocation success in rare plant species.

The fundamental goal of a rare plant translocation is to create self-sustaining populations with the evolutionary resilience to persist in the long term. Yet, most plant translocation syntheses focus on a few factors influencing short-term benchmarks of success (e.g., survival and reproduction). Short-term benchmarks can be misleading when trying to infer future growth and viability because the factors that promote establishment may differ from those required for long-term persistence. We assembled a large (n = 275) and broadly representative data set of well-documented and monitored (7.9 years on average) at-risk plant translocations to identify the most important site attributes, management techniques, and species' traits for six life-cycle benchmarks and population metrics of translocation success. We used the random forest algorithm to quantify the relative importance of 29 predictor variables for each metric of success. Drivers of translocation outcomes varied across time frames and success metrics. Management techniques had the greatest relative influence on the attainment of life-cycle benchmarks and short-term population trends, whereas site attributes and species' traits were more important for population persistence and long-term trends. Specifically, large founder sizes increased the potential for reproduction and recruitment into the next generation, whereas declining habitat quality and the outplanting of species with low seed production led to increased extinction risks and a reduction in potential reproductive output in the long-term, respectively. We also detected novel interactions between some of the most important drivers, such as an increased probability of next-generation recruitment in species with greater seed production rates, but only when coupled with large founder sizes. Because most significant barriers to plant translocation success can be overcome by improving techniques or resolving site-level issues through early intervention and management, we suggest that by combining long-term monitoring with adaptive management, translocation programs can enhance the prospects of achieving long-term success.

Identificación de pronosticadores del éxito de reubicación en especies raras de plantas Resumen El objetivo fundamental de la reubicación de plantas raras es la creación de poblaciones autosuficientes con resiliencia evolutiva que persistan a la larga. De todas maneras, la mayoría de las síntesis de estas reubicaciones se enfocan en unos cuantos factores que influyen sobre los parámetros a corto plazo del éxito (supervivencia y reproducción). Los parámetros a corto plazo pueden ser engañosos si se intenta inferir el crecimiento y la viabilidad en el futuro ya que los factores que promueven el establecimiento pueden diferir de aquellos requeridos para la persistencia a largo plazo. Ensamblamos un conjunto grande de datos representativos en general (n = 275) de las reubicaciones de plantas en riesgo bien documentadas y monitoreadas (7.9 años en promedio) para identificar los atributos de sitio más importantes, las técnicas de manejo y los rasgos de las especies para seis parámetros de ciclos de vida y medidas poblacionales del éxito de reubicación. Usamos el algoritmo de bosque aleatorio para cuantificar la importancia relativa de las 29 variables de pronosticadores para cada medida del éxito. Los factores en los resultados de las reubicaciones variaron con los marcos temporales y las medidas de éxito. Las técnicas de manejo tuvieron la mayor influencia relativa sobre la obtención de parámetros de ciclos de vida y tendencias poblacionales a corto plazo, mientras que los atributos de sitio y los rasgos de la especie fueron más importantes para la persistencia poblacional y las tendencias a largo plazo. En específico, las grandes cantidades de fundadores incrementaron el potencial de reproducción y reclutamiento de la siguiente generación, mientras que la declinación de la calidad del hábitat incrementó el riesgo de extinción y el trasplante de especies con baja producción de semillas redujo el rendimiento del potencial reproductivo a la larga. También detectamos interacciones novedosas entre algunos de los factores más importantes, como el aumento en la probabilidad del reclutamiento en la siguiente generación en especies con tasas mayores de producción de semillas, pero sólo cuando se emparejó con grandes cantidades de fundadores. Ya que las barreras más significativas para el éxito de la reubicación de plantas pueden superarse al mejorar las técnicas o resolver los temas a nivel de sitio por medio de un manejo y una intervención temprana, sugerimos que con la combinación del monitoreo a largo plazo con el manejo adaptativo los programas de reubicación pueden aumentar el prospecto de lograr el éxito a largo plazo.

Climate suitability as a predictor of conservation translocation failure.

The continuing decline and loss of biodiversity has caused an increase in the use of interventionist conservation tools, such as translocation. However, many translocation attempts fail to establish viable populations, with poor release site selection often flagged as an inhibitor of success. We used species distribution models (SDMs) to predict the climate suitability of 102 release sites for amphibians, reptiles, and terrestrial insects and compared suitability predictions between successful and failed attempts. We then quantified the importance of climate suitability relative to 5 other variables frequently considered in the literature as important determinants of translocation success: number of release years, number of individuals released, life stage released, origin of the source population, and position of the release site relative to the species' range. Probability of translocation success increased as predicted climate suitability increased and this effect was the strongest among the variables we considered, accounting for 48.3% of the variation in translocation outcome. These findings should encourage greater consideration of climate suitability when selecting release sites for conservation translocations and we advocate the use of SDMs as an effective way to do this.

Idoneidad Climática como Pronosticador del Fracaso de la Reubicación por Conservación Resumen La continua declinación y pérdida de la biodiversidad ha ocasionado un incremento en el uso de herramientas intervencionistas de conservación como la reubicación. Sin embargo, muchos intentos de reubicación fracasan en el establecimiento de poblaciones viables, y generalmente se identifica a la mala selección de sitios de liberación como el inhibidor del éxito. Usamos modelos de distribución de especies (MDE) para predecir la idoneidad climática de 102 sitios de liberación para anfibios, reptiles e insectos terrestres y comparamos las predicciones de idoneidad entre los intentos fallidos y los exitosos. Después cuantificamos la importancia de la idoneidad climática en relación a otras cinco variables consideradas frecuentemente en la literatura como determinantes importantes del éxito de la reubicación: el número de años de liberaciones, el número de individuos liberados, la etapa de vida durante la liberación, la fuente de la población de origen y la posición del sitio de liberación en relación a la extensión de la especie. La probabilidad del éxito de la reubicación incrementó conforme aumentó la idoneidad climática pronosticada y este efecto fue el más fuerte entre las variables que consideramos, representando el 48.3% de la variación del resultado de la reubicación. Estos hallazgos deberían promover una mayor consideración de la idoneidad climática cuando se seleccionan sitios de liberación para reubicaciones por conservación y abogamos que el uso de los MDE es un método efectivo para hacer esto.

Effects of life history and reproduction on recruitment time lags in reintroductions of rare plants.

Reintroductions are important components of conservation and recovery programs for rare plant species, but their long-term success rates are poorly understood. Previous reviews of plant reintroductions focused on short-term (e.g., ≤3 years) survival and flowering of founder individuals rather than on benchmarks of intergenerational persistence, such as seedling recruitment. However, short-term metrics may obscure outcomes because the unique demographic properties of reintroductions, including small size and unstable stage structure, could create lags in population growth. We used time-to-event analysis on a database of unusually well-monitored and long-term (4-28 years) reintroductions of 27 rare plant species to test whether life-history traits and population characteristics of reintroductions create time-lagged responses in seedling recruitment (i.e., recruitment time lags [RTLs]), an important benchmark of success and indicator of persistence in reintroduced populations. Recruitment time lags were highly variable among reintroductions, ranging from <1 to 17 years after installation. Recruitment patterns matched predictions from life-history theory with short-lived species (fast species) exhibiting consistently shorter and less variable RTLs than long-lived species (slow species). Long RTLs occurred in long-lived herbs, especially in grasslands, whereas short RTLs occurred in short-lived subtropical woody plants and annual herbs. Across plant life histories, as reproductive adult abundance increased, RTLs decreased. Highly variable RTLs were observed in species with multiple reintroduction events, suggesting local processes are just as important as life-history strategy in determining reintroduction outcomes. Time lags in restoration outcomes highlight the need to scale success benchmarks in reintroduction monitoring programs with plant life-history strategies and the unique demographic properties of restored populations. Drawing conclusions on the long-term success of plant reintroduction programs is premature given that demographic processes in species with slow life-histories take decades to unfold.

Efectos de la Historia de Vida y la Reproducción sobre las Demoras en el Tiempo de Reclutamiento en la Reintroducción de Plantas Raras Resumen Las reintroducciones son componentes importantes de los programas de conservación y recuperación de especies raras de plantas, pero las tasas de éxito a largo plazo cuentan con muy poco entendimiento. Las revisiones previas de las reintroducciones de plantas se han enfocado en la supervivencia a corto plazo (p. ej.: ≤ 3 años) y en el florecimiento de individuos fundadores en lugar de enfocarse en puntos de referencia para la persistencia inter-generacional, como el reclutamiento de plántulas. Sin embargo, las medidas a corto plazo pueden ocultar los resultados ya que las propiedades demográficas únicas de las reintroducciones, incluyendo el menor tamaño y la estructura inestable de estadio, podrían crear demoras en el crecimiento poblacional. Usamos un análisis de tiempo-para-evento en una base de datos de reintroducciones inusualmente bien monitoreadas y de largo plazo (4-28 años) de 27 especies raras de plantas para probar si los atributos de la historia de vida y las características poblacionales de la reintroducción crean respuestas con demoras temporales en el reclutamiento de plántulas (es decir, demoras temporales en el reclutamiento), un punto de referencia importante para el éxito y un indicador de la persistencia en poblaciones reintroducidas. Las demoras temporales de reclutamiento (RTLs, en inglés) fueron muy variables entre las reintroducciones, abarcando desde <1 hasta 17 años después de la instalación. Los patrones de reclutamiento se acoplaron a las predicciones de la teoría de historias de vida, donde las especies de vida corta (especies rápidas) exhibieron RTLs consistentemente más cortas y menos variables que las especies de vida larga (especies lentas). Las RTLs largas ocurrieron en hierbas de vida larga, especialmente en los pastizales, mientras que las RTLs cortas ocurrieron en plantas leñosas subtropicales de vida corta y en hierbas anuales. En todas las historias de vida de las plantas, conforme incrementó la abundancia de adultos reproductivos, las RTLs disminuyeron. Se observaron RTLs altamente variables en las especies con eventos de reintroducción múltiples, lo que sugiere que los procesos locales son igual de importantes que la estrategia de historia de vida para determinar los resultados de las reintroducciones. Las demoras temporales en los resultados de restauración resaltan la necesidad de poner a escala los puntos de referencia de éxito en los programas de monitoreo de reintroducciones que tengan estrategias de historia de vida de las plantas y las propiedades demográficas únicas de las poblaciones restauradas. La obtención de conclusiones sobre el éxito a largo plazo de los programas de reintroducción de plantas es algo prematuro ya que los procesos demográficos de especies con historias de vida lentas tardan décadas en desarrollarse.

Center for Plant Conservation's Best Practice Guidelines for the reintroduction of rare plants.

Recent estimates indicate that one-fifth of botanical species worldwide are considered at risk of becoming extinct in the wild. One available strategy for conserving many rare plant species is reintroduction, which holds much promise especially when carefully planned by following guidelines and when monitored long-term. We review the Center for Plant Conservation Best Reintroduction Practice Guidelines and highlight important components for planning plant reintroductions. Before attempting reintroductions practitioners should justify them, should consider alternative conservation strategies, understand threats, and ensure that these threats are absent from any recipient site. Planning a reintroduction requires considering legal and logistic parameters as well as target species and recipient site attributes. Carefully selecting the genetic composition of founders, founder population size, and recipient site will influence establishment and population growth. Whenever possible practitioners should conduct reintroductions as experiments and publish results. To document whether populations are sustainable will require long-term monitoring for decades, therefore planning an appropriate monitoring technique for the taxon must consider current and future needs. Botanical gardens can play a leading role in developing the science and practice of plant reintroduction.

Differential response to soil salinity in endangered key tree cactus: implications for survival in a changing climate.

Understanding reasons for biodiversity loss is essential for developing conservation and management strategies and is becoming increasingly urgent with climate change. Growing at elevations <1.4 m in the Florida Keys, USA, the endangered Key tree cactus (Pilosocereus robinii) experienced 84 percent loss of total stems from 1994 to 2007. The most severe losses of 99 and 88 percent stems occurred in the largest populations in the Lower Keys, where nine storms with high wind velocities and storm surges, occurred during this period. In contrast, three populations had substantial stem proliferation. To evaluate possible mortality factors related to changes in climate or forest structure, we examined habitat variables: soil salinity, elevation, canopy cover, and habitat structure near 16 dying or dead and 18 living plants growing in the Lower Keys. Soil salinity and elevation were the preliminary factors that discriminated live and dead plants. Soil salinity was 1.5 times greater, but elevation was 12 cm higher near dead plants than near live plants. However, distribution-wide stem loss was not significantly related to salinity or elevation. Controlled salinity trials indicated that salt tolerance to levels above 40 mM NaCl was related to maternal origin. Salt sensitive plants from the Lower Keys had less stem growth, lower root:shoot ratios, lower potassium: sodium ratios and lower recovery rate, but higher δ (13)C than a salt tolerant lineage of unknown origin. Unraveling the genetic structure of salt tolerant and salt sensitive lineages in the Florida Keys will require further genetic tests. Worldwide rare species restricted to fragmented, low-elevation island habitats, with little or no connection to higher ground will face challenges from climate change-related factors. These great conservation challenges will require traditional conservation actions and possibly managed relocation that must be informed by studies such as these.

Using population viability analysis to predict the effects of climate change on the extinction risk of an endangered limestone endemic shrub, Arizona cliffrose.

The threat of global warming to rare species is a growing concern, yet few studies have predicted its effects on rare populations. Using demographic data gathered in both drought and nondrought years between 1996-2003 in central Arizona upper Sonoran Desert, we modeled population viability for the federally endangered Purshia subintegra (Kearney) Henrickson (Arizona cliffrose). We used deterministic matrix projection models and stochastic models simulating weather conditions during our study, given historical weather variation and under scenarios of increased aridity. Our models suggest that the P. subintegra population in Verde Valley is slowly declining and will be at greater risk of extinction with increased aridity. Across patches at a fine spatial scale, demographic performance was associated with environmental factors. Moist sites (patches with the highest soil moisture, lowest sand content, and most northern aspects) had the highest densities, highest seedling recruitment, and highest risk of extinction over the shortest time span. Extinction risk in moist sites was exacerbated by higher variance in recruitment and mortality. Dry sites had higher cumulative adult survival and lower extinction risk but negative growth rates. Steps necessary for the conservation of the species include introductions at more northern latitudes and in situ manipulations to enhance seedling recruitment and plant survival. We demonstrate that fine spatial-scale modeling is necessary to predict where patches with highest extinction risk or potential refugia for rare species may occur Because current climate projections for the 21st century imply range shifts at rates of 300 to 500 km/century, which are beyond even exceptional examples of shifts in the fossil record of 100-150 km, it is likely that preservation of many rare species will require human intervention and a long-term commitment. Global warming conditions are likely to reduce the carrying capacity of many rare species' habitats.

Seedling recruitment and survival of an endangered limestone endemic in its natural habitat and experimental reintroduction sites.

The largest and most fecund population of the endangered Purshia subintegra is restricted to limestone mesas in Verde Valley, Arizona, USA, where habitat destruction is imminent. To examine factors limiting its distribution and potential for expansion, we compared recruitment and survival of seedlings growing in soils from occupied and unoccupied habitat in caged field experiments and compared survival of caged and wild seedling cohorts from 1998 to 2003. In field tests, seeds germinated in soils from occupied and unoccupied habitats. Seedling survival, however, was greatest in currently occupied habitat and dropped to zero in some unoccupied habitats with the onset of severe drought. Among 16 factors measured, soil moisture significantly explained between 62% and 71% of the variation in recruitment in both wild and caged plots. Shrubs conferred protection to wild seedlings, but decreased caged seedling survival. For 5 yr following germination, caged seedlings had greater survival than natural seedling cohorts indicating that reintroduction was comparatively more successful than natural recruitment. Expansion of P. subintegra into novel habitats is limited by soil moisture capacity, and this condition varied during the experimental time frame. Reintroductions to limestone mesas are possible and most promising if cages and supplemental watering are used.